Hypomagnetic Fields and Their Multilevel Effects on Living Organisms
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
processes
Review
Hypomagnetic Fields and Their Multilevel Effects on
Living Organisms
Miroslava Sinčák and Jana Sedlakova-Kadukova *
Faculty of Natural Science, University of Cyril and Methodius in Trnava, Nam. J. Herdu 2, 91701 Trnava, Slovakia
* Correspondence: prof.jana.sedlakova@ucm.sk; Tel.: +421-905245200
Abstract: The Earth’s magnetic field is one of the basic abiotic factors in all environments, and
organisms had to adapt to it during evolution. On some occasions, organisms can be confronted with
a significant reduction in a magnetic field, termed a “hypomagnetic field—HMF”, for example, in
buildings with steel reinforcement or during interplanetary flight. However, the effects of HMFs
on living organisms are still largely unclear. Experimental studies have mostly focused on the
human and rodent models. Due to the small number of publications, the effects of HMFs are
mostly random, although we detected some similarities. Likely, HMFs can modify cell signalling
by affecting the contents of ions (e.g., calcium) or the ROS level, which participate in cell signal
transduction. Additionally, HMFs have different effects on the growth or functions of organ systems
in different organisms, but negative effects on embryonal development have been shown. Embryonal
development is strictly regulated to avoid developmental abnormalities, which have often been
observed when exposed to a HMF. Only a few studies have addressed the effects of HMFs on the
survival of microorganisms. Studying the magnetoreception of microorganisms could be useful to
understand the physical aspects of the magnetoreception of the HMF.
Keywords: hypomagnetic field; magnetic zero; magnetoreception
Citation: Sinčák, M.;
Sedlakova-Kadukova, J.
1. Introduction
Hypomagnetic Fields and Their
Multilevel Effects on Living
Every living organism on Earth has adapted to the geomagnetic field during an evolu-
Organisms. Processes 2023, 11, 282. tionary process lasting billions of years. The presence of a geomagnetic field (approximately
https://doi.org/10.3390/pr11010282 50 uT) is natural to each cell [1]. However, in a few circumstances, organisms can face
the absence of magnetic fields. Understanding its effect can enhance our knowledge of
Academic Editors: Roberto
magnetoreception mechanisms, with applications in space research, biotechnology or
Alonso González Lezcano,
medicine. The terms “hypomagnetic”, “conditionally zero magnetic field” or “magnetic
Francesco Nocera and Rosa
vacuum” generally refer to fields with a magnetic flux density (B) below 100 nT [2], but
Giuseppina Caponetto
according to some authors, we can speak of a magnetic field weaker than 5 µT as being
Received: 13 December 2022 hypomagnetic [3].
Revised: 9 January 2023 Hypomagnetic fields (HMFs) commonly occur in the interplanetary space of the
Accepted: 12 January 2023 solar system and fluctuate in the range of several nanoteslas (nT). For example, the lunar
Published: 16 January 2023 magnetic field is less than 300 nT, and the magnetic field on Mars is approximately 1 µT [3].
The planetary magnetic field of Mars is extremely small, and the planetary magnetic field
of Venus is practically non-existing [4] (Figure 1).
New technologies are currently being developed to enable space exploration and
Copyright: © 2023 by the authors.
interplanetary flights. In the future, organisms will be exposed to a HMF during space
Licensee MDPI, Basel, Switzerland.
travels, which is significantly weaker than the geomagnetic field (GMF) and expected to
This article is an open access article
have diverse biological effects. During these travels, organisms will be exposed to tedious
distributed under the terms and
conditions of the Creative Commons
periods of a HMF that is approximately 10,000 times weaker than the Earth’s magnetic
Attribution (CC BY) license (https://
field, ranging from 0.1 to 1 nT [5]. However, attenuation of the Earth’s magnetic field is
creativecommons.org/licenses/by/ not limited to staying in space but occurs in daily life, for example, in buildings with steel
4.0/).
Processes 2023, 11, 282. https://doi.org/10.3390/pr11010282 https://www.mdpi.com/journal/processesProcesses 2023, 11, 282 2 of 13
walls or steel reinforcement [2]. Building walls are a natural shield against low- and high-
frequency electromagnetic fields. However, a magnetic field (such as a geomagnetic field)
is more difficult to shield. In contrast to radiofrequency and low-frequency electric fields,
thin sheets of metal have no effect on magnetic fields [6]. However, there is evidence that
buildings with steel in their construction magnetise and deform the natural geomagnetic
Processes 2023, 11, x FOR PEER REVIEW 2 size
field [5], causing an even 50-fold magnetic field attenuation according to the building of 13
and the complexity of the steel [7].
Figure1.1.Presence
Figure Presenceof
ofhypomagnetic
hypomagneticfield
fieldin
inthe
thesolar
solarsystem
system[3].
[3].
New technologies
Hypomagnetic fieldsarecan
currently being effects
have various developed to enable space
on organisms, exploration
although and in-
the underlying
terplanetary remain
mechanisms flights. unknown.
In the future, organisms
Erdman willsuggest
et al. [8] be exposed to amagnetoreception
that the HMF during spaceoftrav- the
els, which is significantly weaker than the geomagnetic field
HMF differs among different organisms. The authors assume that the magnetoreception of (GMF) and expected to have
diverse
the HMFbiological effects.mechanism
is a nonspecific During these andtravels,
manifestsorganisms
in highly will be exposed
different to tedious
biological systems pe-
riods
as of arandom
mostly HMF that is approximately
reactions as a result 10,000 timesinteraction
of magnetic weaker than withthemagnetic
Earth’s magnetic
momentsfield, at a
ranging level.
physical from This0.1 to 1 nT [5].
moment, However,
which attenuation
is present of the Earth’s
in each molecule, magnetic
could transfer thefield is not
magnetic
limited
signal at to
thestaying
level ofindownstream
space but occurs in daily
biochemical life, for
events [2]. example, in buildings with steel
wallsInor steel
this reinforcement
study, we summarise [2].information
Building walls about arethea natural
observedshield against
biological low-
effects ofand high-
the HMF
on eukaryotic and prokaryotic organisms and show the possible
frequency electromagnetic fields. However, a magnetic field (such as a geomagnetic field)underlying mechanisms.
is more difficult to shield. In contrast to radiofrequency and low-frequency electric fields,
2. Materials
thin sheets ofand Methods
metal have no effect on magnetic fields [6]. However, there is evidence that
We used
buildings withthe scientific
steel in their databases
construction PubMed
magnetise and andScienceDirect
deform thetonatural
select geomagnetic
papers that
contained the terms
field [5], causing an “hypomagnetic”,
even 50-fold magnetic “magnetic zero”, “magnetic
field attenuation vacuum”
according to theor “magnetic
building size
shielding” in their titles, abstracts
and the complexity of the steel [7]. and keywords. This gave, after a subsequent semantic
control, 65 experimental
Hypomagnetic fieldsandcantheoretical
have various articles that
effects onincluded
organisms, original results
although thesuitable
underlying for
further investigation. This type of search was repeated with
mechanisms remain unknown. Erdman et al. [8] suggest that the magnetoreception of the each new relevant article
iteratively
HMF differs until no new
among articlesorganisms.
different could be detected.
The authors assume that the magnetoreception
of the HMF is a nonspecific mechanism and manifests in highly different biological sys-
3. Mechanisms of Magnetoreception of HMFs
tems as mostly random reactions as a result of magnetic interaction with magnetic mo-
mentsMagnetoreception
at a physical level. is This
the universal
moment, abilitywhich is of present
a biological system
in each to detect
molecule, could magnetic
transfer
and electromagnetic fields, although it may manifest
the magnetic signal at the level of downstream biochemical events [2] itself differently in different organ-
isms. InAny
this study, we summarise information about the observed biological effects ways,
changes in magnetic field intensity may affect the organisms in many of the
including the basic metabolism
HMF on eukaryotic and prokaryotic of prokaryotic
organisms and andeukaryotic
show thecells [8]. Magnetoreception
possible underlying mech-
relates
anisms.not only to geomagnetic fields and higher magnetic and electromagnetic fields,
but it also explains the perception of HMFs. The hypothesis of nonspecific nonthermal
magnetoreception
2. Materials and Methods on the physical level has not been studied since none of those has yet
been identified experimentally. Typical for hypomagnetic magnetoreception experiments
We used the scientific databases PubMed and ScienceDirect to select papers that con-
is a high sensitivity to the physical, chemical and physiological conditions, as well as a
tained the terms “hypomagnetic”, “magnetic zero”, “magnetic vacuum” or “magnetic
low reproducibility [2] and a great variety of effects in different organisms. It has not
shielding” in their titles, abstracts and keywords. This gave, after a subsequent semantic
yet been possible to establish any common conditions controlling the magnetic effects
control, 65 experimental and theoretical articles that included original results suitable for
in different organisms or populations rather than in their individual forms [9]. Several
further investigation.
mechanisms have beenThis type ofthat
described search
could was repeated
explain with each new
the mechanism relevant article it-
of magnetoreception,
eratively until no new articles could be detected.
such as the cyclotron resonance model, macroscopic charged vortices in the cytoplasm and
the parametric resonance model, among others [10]. The most likely physical mechanisms
3. Mechanisms of Magnetoreception of HMFs
Magnetoreception is the universal ability of a biological system to detect magnetic
and electromagnetic fields, although it may manifest itself differently in different organ-
isms. Any changes in magnetic field intensity may affect the organisms in many ways,
including the basic metabolism of prokaryotic and eukaryotic cells [8]. MagnetoreceptionProcesses 2023, 11, 282 3 of 13
with expected biological responses are: (i) the radical pair mechanism, (ii) the universal
physical mechanism and (iii) the molecular gyroscope mechanism. However, according
to Binhi and Prato [2], the radical pair mechanism is unlikely to explain all HMF effects
on living organisms. The authors assume that the universal physical mechanism and the
molecular gyroscope mechanism are more accurate.
These primary physical mechanisms can lead to secondary biophysical responses,
which can include changes in ROS concentrations, Ca2+ ion homeostasis or influence
enzymes that are involved in the electron transport chain in mitochondria or in cell cy-
cle promotion.
1. Radical pair mechanism
Traditionally, radicals (for example, reactive oxygen species (ROS)) are considered
harmful because they can cause cell death via oxidative intracellular damage in the
metabolism of sugars, fats and nucleic acids. Several studies have also shown the im-
portance of ROS in intracellular signalling cascades such as apoptosis initiation [11–13].
Radicals are magnetic because an electron (along with a proton and a neutron) has a
property known as spin or, more precisely, a spin momentum [14].
The radical pair consists of two radicals that have been formed simultaneously, usually
by a chemical reaction. The spins of two unpaired electrons can be either parallel to each
other (↑↑ which gives S = 1) or anti-parallel (↑↓, which gives S = 0, where S is the spin
quantum number). The two forms of the electron pair are therefore known as triplet (S = 1)
and singlet (S = 0) [15]. Influencing either singlet or triplet formations of electron pairs
could be associated with the presence of an external magnetic field and leads to a longer
life of the radical pairs (triplet states) [16].
This mechanism can cause a difference in the stability of radical pairs and affects the
shift of the chemical reaction equilibrium. Thus, during the formation of radical pairs,
external magnetic fields change the recombination rate of these radical pairs, which in turn
changes the concentration of radicals such as O2 • and molecules such as H2 O2 [17]. In
general, the coupling between unpaired electrons and nuclei in each fragment of a radical
pair can be achieved by magnetic fields in the range of 10 µT–3 mT [18]. Magnetic fields
could interact with the magnetic moments of radical pairs at physical levels, which are
ubiquitous in macromolecules with unpaired electrons, protons, paramagnetic ions or other
magnetic nuclei in biological cells, and then transmit the magnetic signal to subsequent
biochemical events such as cell oxidative stress reactions. This procedure would therefore
lead to highly different biological observables and mostly random reactions [19].
This mechanism does not have frequency selectivity because the development of a
magnetosensitive spin state occurs over an extremely short life of the radical pair, usu-
ally in the order of 10−9 –10−7 s [20]. Many authors explain the observed results by this
mechanism [21–23].
2. Universal physical mechanism
The rotation of magnetic moments in a magnetic field precedes any biophysical or
biochemical mechanism of magnetoreception and largely determines the spectral and
nonlinear characteristics of the biological effect of the field. The mechanism is based on the
external magnetic field, which influences the magnetic moment of the molecules and leads
to the terminal relaxation of the magnetic moment [19]. Magnetic relaxation is known as
the approach to equilibrium after a magnetic system was exposed to magnetic field change.
Relaxation processes allow nuclear spins to return to equilibrium following a magnetic
disturbance [24].
The biological effect is observed only when changes in the magnetic momentum
dynamics go through the stages of transformation at the biochemical, physiological and
biological levels of the system. A special characteristic of this mechanism is that it predicts
the effects of weak magnetic fields but also those of electromagnetic fields induced by
alternating electric currents (ACs) in the same biological system [2].
3. Molecular gyroscope mechanismProcesses 2023, 11, 282 4 of 13
The molecular gyroscope mechanism can be explained as the rotation of large frag-
ments of macromolecules or amino acid residues with a distributed electric charge. This
movement can be influenced by a magnetic field.
In some stages of protein assembly, in the final stage of their synthesis, virtual cavities
without water molecules, of the order of 1 nm or less, may occur in the protein [25]. In these
cavities, amino acid residues (molecular gyroscopes) rotate over milliseconds, searching
for the best position. As a result of such rotation, a magnetic moment interacts with an
external magnetic field [2]. The magnetic field affects these rotations, which results in
possible changes in protein folding. The folding of protein chains is an evolutionarily
conserved process, and improper folding can prevent a protein from performing its specific
function [26]. Mostly, random changes in the proteome of the cell can explain various
biological responses after HMF exposure.
4. Influences of HMFs on Organisms
In many areas, the biological effects of HMFs are contradictory, which might be
explained by the length of exposure to the HMF. The authors of [27] reported that exposure
to a HMF for a shorter time (1 h) could promote cell respiration, but a longer exposure time
(6 h) has an inhibitory effect.
Another parameter causing conflicting results may be the method of generating the
HMF. The authors used either the shielding of the present HMF or its compensation
by another magnetic field, which may have caused a different result. For example, the
production of free radicals caused by direct-current (DC) HMFs differs from the effect of
AC HMFs. A similar difference was observed when the HMF was induced by a static field
or a variable frequency-alternating magnetic field [28].
The type of organism is an important factor of the HMF effect [29]. Not only does the
biological effect of HMFs vary between plant and animal cells, but according to Binhi and
Prato [2], there are different targets of HMFs for different organisms or even for individuals
of the same species. The observed effect of the HMF differs between eukaryotic and
prokaryotic organisms, even in plant and animal cells. Few effects of HMF exposure could
be similar for various organisms and are on the level of individual ions and proteins; they
are generally related to cell signalling.
Regarding the spectrum of the hypomagnetic effect in various types of organisms
according to their basic differences in structure and life cycle, we will separately discuss
plant, animal and prokaryotic organisms.
4.1. Animals and Animal Cell Cultures
The observed effects can differ at various levels of the organization of the living
organism. According to the observations described in various studies, we will discuss cell
transport and respiration in a separate subsection (Section 4.1.1), and subsequently, we will
discuss animals at the level of the organism or organ systems (Section 4.1.2).
4.1.1. Cell Transport and Respiration
The effects of the HMF on a single-cell level may include the effect on ion transport
and concentration as well as cellular respiration (Table 1).
Table 1. Impact of hypomagnetic field on cell transport and metabolism (B—magnetic flux density in
Tesla (T)).
Hypomagnetic Field Properties
Impact on Effect
Organism Mechanism B (nT) Duration References
Mineral density
Reduction Sprague-Dawley rats ShieldingProcesses 2023, 11, 282 5 of 13
Table 1. Cont.
Hypomagnetic Field Properties
Impact on Effect
Organism Mechanism B (nT) Duration References
Ca2+ dependent Enzymes from fish
Inactivation Compensation 1h [32]
proteases and invertebrates
The concentration Fur of laboratory
No effect ShieldingProcesses 2023, 11, 282 6 of 13
However, the mechanism by which the level of ROS is modulated by the magnetic
field remains unclear. It is assumed that weak magnetic fields can alter the free radical
level response and, consequently, affect specific cellular functions and inhibit or reduce
cell growth [43]. In addition to metabolic changes, it is possible to consider changes at the
morphological level, namely the accumulation of lipid bodies, the development of a lytic
compartment (vacuoles and cytosegresomes) and the reduction of phytoferritin in plastids
after HMF exposure [41].
4.1.2. Animals
On the level of the whole organism, studies dealing with HMFs mostly focus on
animals, humans, tissue cultures and embryos. The most common areas of study are
the influences of HMFs on prenatal development as well as cardiovascular and nervous
systems (Table 2).
Table 2. Impact of hypomagnetic field on animal neural systems (B—magnetic flux density in
Tesla (T)).
Hypomagnetic Field Properties
Impact on Effect Organism Mechanism of
B (nT) Duration References
Generation
Every 3 days/
ROS levels Reduction Mouse (C57BL/6 J), males Shielding 170 [23]
150 days
Peritoneal mice
ROS levels Reduction Shielding 20 1.5 h [21]
neutrophils
Primary neural
Growth Promotion progenitor/mouse Shielding 0–200 7 days [42]
stem cells
ROS levels Reduction Human cells of neuroblast Shielding 0–200 16 h [44]
ROS genes
Reduction Mouse (C57BL/6 J), males Shielding 170 3 day/150 days [23]
expression
Reduction
Gene expression (down- Human neuroblast cells CompensationProcesses 2023, 11, 282 7 of 13
Table 2. Cont.
Hypomagnetic Field Properties
Impact on Effect Organism Mechanism of
B (nT) Duration References
Generation
Generational
Fertility Reduction Nilaparvata lugens Compensation 0–1060 [58]
period
Production of
abnormal Promotion Xenopus larvae Shielding 104 ± 12.6 4 days [59]
embryoys
Life cycle Reduction
Fertility NMRI mouse zygotes Shielding 200 12 days [60]
and survival (sterility)
Abortion Promotion Pregnant NMRI mice Shielding 200 3–12 days [60]
Survival of cells Immortalised human
Promotion ShieldingProcesses 2023, 11, 282 8 of 13
function. These results suggest the involvement of the MAPK pathway and cryptochrome
in the early biological responses to the presence of a HMF [45].
In addition to the effects on the neural system, effects of the HMF on the cardiovascular
system have been observed. Capillary blood velocity increased by 17%, cardio intervals
increased by 88.7% [51], and capillary circulation rate increased by 22.4% [52] during HMF
exposure. At the end of exposure, diastolic blood pressure dropped considerably relative to
mid-exposure values, whereas systolic blood pressure, on the contrary, showed a significant
increase [52]. One of the crucial parameters which influence the observed effects of HMFs
is exposure time. Both previous studies claim to have simulated hypomagnetic conditions
during interplanetary flight, but the time of HMF exposure was only 60 min. We assume
that the time of exposure was not sufficient to demonstrate hypomagnetic conditions
during a longer stay in space. In comparison, in two studies with a longer exposure time
of 72 h [53] and up to 4 weeks [54], the authors recorded an increase in haemolysis and
the weakening of the deformation and aggregation properties of human blood, along
with a reduction in enzymatic activities. The reduction of these enzyme activities and the
promotion of haemolysis can be related to increased protein denaturation and decreased
efficiency of the proteolytic system [53].
4.2. Plants
Recent studies have shown that plants respond to near-zero magnetic fields through
morphological and developmental changes, including delays in flowering time and germi-
nation [64], breath conductivity, chlorophyll content [65], photoreceptor involvement [66]
and changes in auxin [67], and gibberellin concentrations [68] (Table 3).
Table 3. Impact of hypomagnetic field on plants (B—magnetic flux density in Tesla (T)).
Hypomagnetic Field Properties
Impact on Effect Organism Mechanism of
B (nT) Duration References
Generation
Growth Reduction Glycine max Shielding 111 ± 15 24 h [69]
Growth Reduction Arabidopsis thaliana Compensation 0–1330 35 days [70]
Growth Reduction Arabidopsis thaliana Compensation 40–44 96 h [71]
Epicotyl
Promotion Pisum sativum Shielding - 24 h [72]
elongation
Gene expansion Reduction Arabidopsis thaliana Compensation 0–1330 33 days [68]
Activity of
photoreceptors Reduction Arabidopsis thaliana Compensation 40 3h [64]
phyA
Activity of phyB
Promotion Arabidopsis thaliana Compensation 40 3h [64]
photoreceptors
The content of
Reduction Arabidopsis thaliana Compensation 0–1330 33 days [67]
auxin in flower
Gene expression
(associated with Promotion Arabidopsis thaliana Compensation 50 33 days [73]
flowering)
Auxin content
Promotion Arabidopsis thaliana Compensation 1–1330 33 days [67]
in roots
Iron intake
Reduction Arabidopsis thaliana Compensation 40–44 96 h [71]
by roots
Concentration of Pisum sativum
Promotion Shielding 0.5–2 3 days [41]
Ca2+ ions (root system)Processes 2023, 11, 282 9 of 13
The HMF can either have inhibitory or stimulating effects on plants, depending on
the part of the growth to which the plant is exposed. Hypomagnetic fields can inhibit [41]
but also promote vegetative growth, e.g., by increasing the percentage of the germination
rate [69]. On the other hand, they may have a reducing effect on reproductive growth
by inhibiting seed production [70]. The magnetic field, in this case, is thought to affect
the activity of cryptochromes and their gene expressions [64,74]. Plant hormones are also
involved in cryptochrome-mediated flowering. Exposure to HMFs reduces the gibberellin
content and the expression of their biosynthetic genes in wild-type Arabidopsis thaliana
but not in the cryptochrome mutant strain (cry1/cry2). Similar results have been obtained
for another plant hormone, auxin [67].
As in the case of animal cells, changes in the ion concentrations of some nutrients
(NH4 + , K+ , Ca2+ Mg2+ , Cl− , SO4 2− , NO3 − and PO4 3− ) in plant cells after exposure of the
A. thaliana root system to the HMF were recorded. A few minutes of exposure to a zero
magnetic field resulted in a significant reduction in the intake of all studied nutrient ions,
which can be explained by the existence of a plant magnetoreceptor responding to the
HMF by modulating mineral nutrient transport genes. According to Narayan et al. [75], the
response to an almost zero magnetic field is rapid, suggesting that some ion channels and all
transport activities may not necessarily be related to gene expression. Ion channel changes
have been reported in other studies and may influence flowering time [64], photoreceptor
signaling [76], and seed germination [77].
In plant cells exposed to HMFs, the functional activity of the genome declined in
the early pre-replication period. The HMF can intensify protein synthesis. At the ultra-
structural level, changes in condensed chromatin distribution and nuclear compaction,
the accumulation of lipid bodies, the development of the lytic compartment (vacuoles,
cytosegresomas and paramural bodies), and the reduction of phytoferritin in plastids in
meristem cells have been observed in pea roots [39].
In contrast to the animal cell, where the HMF stimulated proliferation and accelerated
the passage through the G1 phase, the observed effect on the plant cell was the opposite.
The HMF had a negative effect on the speed and progress of the cell cycle. The reproductive
cycle of the cells slowed down due to the expansion of the G1 and G2 phases, whereas the
other phases of the cell cycle remained relatively stable. The HMF also caused a remarkable
decrease in proliferating plant cells (from 68% to 95%) [41].
Tsetlin et al. [78] also recorded remarkable results when they described a synergistic
inhibitory effect of HMF and ionizing radiation (α and γ) on plant germination. This
experiment simulated another environmental parameter to which the plants will be exposed
during interplanetary flights.
4.3. Prokaryotes
Only a few studies have examined the effects of the HMF on microorganisms. Magne-
totactic bacteria, i.e., bacteria capable of perceiving the Earth’s geomagnetic field by means
of magnetosomes, have been investigated most frequently [5] (Table 4).
Table 4. Impact of hypomagnetic field on procaryotic microorganisms (B—magnetic flux density in
Tesla (T)).
Field Properties
Impact on Effect Organism
Mechanism B (nT) Duration References
Growth and number of cells Reduction Magnetotactic bacteria (MO-1) Shielding 2 2 days [79]
Both reduction
Tolerance to antibiotics Escherichia coli Compensation - 6 days [80]
and promotion
Both reduction
Tolerance to antibiotics Pseudomonas and Enterobacter strains Field compensation - 6 days [81]
and promotion
Magnetosome size Promotion Magnetospirillum magneticum AMB-1 Compensation 500 16 h [82]
Gene expression Modification Magnetospirillum magneticum AMB-1 Compensation 500 16 h [82]Processes 2023, 11, 282 10 of 13
Studies on the magnetotactic bacterium Magnetospirillum magneticum AMB-1 have
shown that after 16 h of magnetic compensation (500 nT), AMB-1 synthesises larger magne-
tosomes due to the up-regulation (stimulation) of genes encoding larger magnetosomes
and the down-regulation (inhibition) of genes encoding smaller magnetosomes. The gene
responsible for magA iron transport remained unchanged [82]. Inhibition of the growth
and viability of magnetotactic bacteria (MO-1) after exposure to a 2-nT magnetic field for
2 days has also been noted [79].
In addition to magnetotactic bacteria, changes in antibiotic resistance in human
pathogenic bacteria have been studied. The susceptibility of 26 strains of Escherichia
coli to selected antibiotics was examined after HMF exposure. Susceptibility to antibiotics
(ampicillin, ceftazidime, tetracycline, ofloxacin, and kanamycin) either increased or de-
creased in different strains, depending on the studied drug. The authors detected two types
of E. coli strains: non-sensitive and sensitive to geomagnetic field compensation, which
represents about one-third of the strains. Magneto-sensitive E. coli strains showed modified
minimum inhibitory concentration (MIC) values to two of five tested antibiotics after HMF
exposure [80]. According to Creanga et al. [81], half of the eight tested human pathogen
strains (Pseudomonas and Enterobacter strains) were magnetosensitive and showed a
change in antibiotic susceptibility (increase or decrease, depending on the tested antibiotics)
from 2- to 16-fold.
Ilyin et al. [83] have recently isolated bacteria from the nasopharynx of cosmonauts
after their return to Earth from a space mission. The authors observed multiple decreases
in antibiotic resistance after exposure to space conditions. Although the effect of the HMF
was not especially investigated in this study, its effect on bacterial life is undeniable and
can be related to the observed changes in resistance.
The authors further suggest that the HMF can affect cell metabolism by changing
the ion transport mechanism in cell plasma membranes in the prokaryotic cell, and this
can be applicable in eucaryotic magnetoreception by influencing endoplasmic reticulum
(including ribosomal membranes) and mitochondrial membranes [81].
5. Conclusions
So far, the impacts of HMFs on biological systems have been rarely investigated, and
the exact mechanism of action remains unclear. The authors explain their results by several
theoretical mechanisms, most often by the mechanism of radical pairs which influence the
reactive oxygen species concentration. Experimental studies on HMFs yielded conflicting
results on the development and functioning of the nervous and cardiovascular systems.
However, HMFs are likely to have a negative effect on early developmental stages and
fertility in both plants and animals. The conflicting results may have been due to the
different exposure times, organism types, and methods of creating a HMF, which seem to
be the key factors in the observed biological effects.
However, fewer studies have focused on the effect of the HMF on microorganisms. In
our opinion, it is the research of prokaryotic models that can offer useful insight into the
magnetoreception of the HMF. Based on this review, the level of magnetoreception can take
place at the level of ions, protein complexes, or the cell membrane, and thus, the primary
targets of the HMF could be similar for both prokaryotic and eukaryotic organisms.
Hypomagnetic fields seem to affect cell signaling on the level of ion transport and
ROS, which has been demonstrated for disruptive embryonal development.
Author Contributions: M.S. wrote the paper; J.S.-K. edited the manuscript. All authors have read
and agreed to the published version of the manuscript.
Funding: The work was supported by financial aid from the Slovak Grant Agency project No.
VEGA 1/0018/22.
Data Availability Statement: The manuscript has no associated data.Processes 2023, 11, 282 11 of 13
Conflicts of Interest: The authors declare no conflict of interest or interpretation of data. The funders
had no role in the design of the study; in the collection, analyses, or interpretation of data; in the
writing of the manuscript; or in the decision to publish the results.
References
1. Monteil, C.L.; Lefevre, C.T. Magnetoreception in Microorganisms. Trends Microbiol. 2019, 28, 266–275. [CrossRef] [PubMed]
2. Binhi, V.N.; Prato, F.S. Biological effects of the hypomagnetic field: An analytical review of experiments and theories. PLoS ONE
2017, 12, e0179340. [CrossRef] [PubMed]
3. Mo, W.; Liu, Y.; He, R. Hypomagnetic field, an ignorable environmental factor in space? Sci. China Life Sci. 2014, 57, 726–728.
[CrossRef] [PubMed]
4. Kivelson, M.G.; Bagenal, F. Planetary magnetospheres. In Encyclopedia of the Solar System, 3rd ed.; Elsevier: Amsterdam,
The Netherlands, 2014; Chapter 7, pp. 137–157.
5. Zhang, Z.; Xue, Y.; Yang, J.; Shang, P.; Yuan, X. Biological Effects of Hypomagnetic Field: Ground-Based Data for Space Exploration.
Bioelectromagnetics 2021, 42, 516–531. [CrossRef]
6. Pavlík, M. Compare of shielding effectiveness for building materials. Prz. Elektrotechniczny 2019, 95, 137–140. [CrossRef]
7. Guo, C.; Liu, D. Quantitative Analyses of Magnetic Field Distributions for Buildings of Steel Structure. In Proceedings of the 2012
Sixth International Conference on Electromagnetic Field Problems and Applications, Dalian, China, 19–21 June 2012.
8. Erdmann, W.; Kmita, H.; Kosicki, J.Z.; Kaczmarek, Ł. How the Geomagnetic Field Influences Life on Earth—An Integrated
Approach to Geomagnetobiology. Space Life Sci. 2021, 51, 231–257. [CrossRef]
9. Wajnberg, E.; Acosta-Avalos, D.; Alves, O.C.; de Oliveira, J.F.; Srygley, R.B.; Esquivel, D.M.S. Magnetoreception in eusocial insects:
An update. J. R. Soc. Interface 2010, 7, S207–S225. [CrossRef] [PubMed]
10. Binhi, V.N.; Savin, A.V. Molecular gyroscopes and biological effects of weak extremely low-frequency magnetic fields. Phys. Rev.
E 2002, 65, 051912. [CrossRef]
11. Dröge, W. Free Radicals in the Physiological Control of Cell Function. Physiol. Rev. 2002, 82, 47–95. [CrossRef]
12. Gauron, C.; Rampon, C.; Bouzaffour, M.; Ipendey, E.; Teillon, J.; Volovitch, M.; Vriz, S. Sustained production of ROS triggers
compensatory proliferation and is required for regeneration to proceed. Sci. Rep. 2013, 3, srep02084. [CrossRef]
13. Van Huizen, A.V.; Morton, J.M.; Kinsey, L.J.; Von Kannon, D.G.; Saad, M.A.; Birkholz, T.R.; Czajka, J.M.; Cyrus, J.; Barnes, F.S.;
Beane, W.S. Weak magnetic fields alter stem cell–mediated growth. Sci. Adv. 2019, 5, eaau7201. [CrossRef] [PubMed]
14. Adams, B.; Sinayskiy, I.; Petruccione, F. An open quantum system approach to the radical pair mechanism. Sci. Rep. 2018, 8, 15719.
[CrossRef] [PubMed]
15. Hore, P.J.; Mouritsen, H. The Radical-Pair Mechanism of Magnetoreception. Annu. Rev. Biophys. 2016, 45, 299–344. [CrossRef]
[PubMed]
16. Ruiz-Gómez, M.J.; Sendra-Portero, F.; Martínez-Morillo, M. Effect of 2.45 mT sinusoidal 50 Hz magnetic field on Saccharomyces
cerevisiae strains deficient in DNA strand breaks repair. Int. J. Radiat. Biol. 2010, 86, 602–611. [CrossRef]
17. Barnes, F.; Greenenbaum, B. Some Effects of Weak Magnetic Fields on Biological Systems: RF fields can change radical concentra-
tions and cancer cell growth rates. IEEE Power Electron. Mag. 2016, 3, 60–68. [CrossRef]
18. Brocklehurst, B.; Mclauchlan, K.A. Free radical mechanism for the effects of environmental electromagnetic fields on biological
systems. Int. J. Radiat. Biol. 1996, 69, 3–24. [CrossRef]
19. Binhi, V.N.; Prato, F.S. A physical mechanism of magnetoreception: Extension and analysis. Bioelectromagnetics 2016, 38, 41–52.
[CrossRef] [PubMed]
20. Otsuka, H.; Mitsui, H.; Miura, K.; Okano, K.; Imamoto, Y.; Okano, T. Rapid Oxidation Following Photoreduction in the Avian
Cryptochrome4 Photocycle. Biochemistry 2020, 59, 3615–3625. [CrossRef] [PubMed]
21. Novikov, V.V.; Yablokova, E.V.; Fesenko, E.E. The Effect of a “Zero” Magnetic Field on the Production of Reactive Oxygen Species
in Neutrophils. Biophysics 2018, 63, 365–368. [CrossRef]
22. Yan, M.-M.; Zhang, L.; Cheng, Y.-X.; Sappington, T.W.; Pan, W.-D.; Jiang, X.-F. Effect of a near-zero magnetic field on development
and flight of oriental armyworm (Mythimna separata). J. Integr. Agric. 2021, 20, 1336–1345. [CrossRef]
23. Zhang, B.; Wang, L.; Zhan, A.; Wang, M.; Tian, L.; Guo, W.; Pan, Y. Long-term exposure to a hypomagnetic field attenuates adult
hippocampal neurogenesis and cognition. Nat. Commun. 2021, 12, 1174. [CrossRef] [PubMed]
24. Gupta, A.; Stait-Gardner, T.; Price, W.S. Is It Time to Forgo the Use of the Terms “Spin–Lattice” and “Spin–Spin” Relaxation in
NMR and MRI? J. Phys. Chem. Lett. 2021, 12, 6305–6312. [CrossRef] [PubMed]
25. Zangi, R.; Hagen, M.; Berne, B.J. Effect of Ions on the Hydrophobic Interaction between Two Plates. J. Am. Chem. Soc. 2007,
129, 4678–4686. [CrossRef] [PubMed]
26. Zhao, V.; Jacobs, W.M.; Shakhnovich, E.I. Effect of Protein Structure on Evolution of Cotranslational Folding. Biophys. J. 2020,
119, 1123–1134. [CrossRef]
27. Ogneva, I.V.; Usik, M.A.; Burtseva, M.V.; Biryukov, N.S.; Zhdankina, Y.S.; Sychev, V.N.; Orlov, O.I. Drosophila melanogaster Sperm
under Simulated Microgravity and a Hypomagnetic Field: Motility and Cell Respiration. Int. J. Mol. Sci. 2020, 21, 5985. [CrossRef]
28. Zhang, B.; Tian, L. Reactive Oxygen Species: Potential Regulatory Molecules in Response to Hypomagnetic Field Exposure.
Bioelectromagnetics 2020, 41, 573–580. [CrossRef]Processes 2023, 11, 282 12 of 13
29. Erdmann, W.; Idzikowski, B.; Kowalski, W.; Kosicki, J.Z.; Kaczmarek, Ł. Tolerance of two anhydrobiotic tardigrades Echiniscus
testudo and Milnesium inceptum to hypomagnetic conditions. PeerJ 2021, 9, e10630. [CrossRef]
30. Jia, W.; Fan, Z.; Du, A.; Shi, L. Molecular mechanism of Mare Nectaris and magnetic field on the formation of ethyl carbamate
during 19 years aging of Feng-flavor Baijiu. Food Chem. 2022, 382, 132357. [CrossRef]
31. Tombarkiewicz, B. Effect of long-term geomagnetic field deprivation on the concentration of some elements in the hair of
laboratory rats. Environ. Toxicol. Pharmacol. 2008, 26, 75–79. [CrossRef]
32. Kantserova, N.P.; Krylov, V.V.; Lysenko, L.A.; Ushakova, N.V.; Nemova, N.N. Effects of Hypomagnetic Conditions and Reversed
Geomagnetic Field on Calcium-Dependent Proteases of Invertebrates and Fish. Izv. Atmos. Ocean. Phys. 2017, 53, 719–723.
[CrossRef]
33. Fu, J.-P.; Mo, W.-C.; Liu, Y.; Bartlett, P.F.; He, R.-Q. Elimination of the geomagnetic field stimulates the proliferation of mouse
neural progenitor and stem cells. Protein Cell 2016, 7, 624–637. [CrossRef] [PubMed]
34. Hu, P.D.; Mo, W.C.; Fu, J.P.; Liu, Y.; He, R.Q. Long-term Hypogeomagnetic field exposure reduces muscular mitochondrial
function and exercise capacity in adult male mice. Prog. Biochem. Biophys. 2020, 47, 426–438.
35. Lednev, V.V. Bioeffects of weak static and alternating magnetic fields. Biofizika 1996, 41, 224–232. [PubMed]
36. Krebs, J. Structure, Function and Regulation of the Plasma Membrane Calcium Pump in Health and Disease. Int. J. Mol. Sci. 2022,
23, 1027. [CrossRef] [PubMed]
37. Poniedziałek, B.; Rzymski, P.; Karczewski, J.; Jaroszyk, F.; Wiktorowicz, K. Reactive oxygen species (ROS) production in human
peripheral blood neutrophils exposed in vitro to static magnetic field. Electromagn. Biol. Med. 2013, 32, 560–568.
38. Vergallo, C.; Ahmadi, M.; Mobasheri, H.; Dini, L. Impact of Inhomogeneous Static Magnetic Field (31.7–232.0 mT) Exposure on
Human Neuroblastoma SH-SY5Y Cells during Cisplatin Administration. PLoS ONE 2014, 9, e113530. [CrossRef]
39. Tang, R.; Xu, Y.; Ma, F.; Ren, J.; Shen, S.; Du, Y.; Hou, Y.; Wang, T. Extremely low frequency magnetic fields regulate differentiation
of regulatory T cells: Potential role for ROS-mediated inhibition on AKT. Bioelectromagnetics 2016, 37, 89–98. [CrossRef]
40. Angelova, P.R.; Dinkova-Kostova, A.T.; Abramov, A.Y. Assessment of ROS Production in the Mitochondria of Live Cells. In
Reactive Oxygen Species; Humana: New York, NY, USA, 2021; pp. 33–42. [CrossRef]
41. Belyavskaya, N. Biological effects due to weak magnetic field on plants. Adv. Space Res. 2004, 34, 1566–1574. [CrossRef]
42. Fu, J.-P.; Mo, W.-C.; Liu, Y.; He, R.-Q. Decline of cell viability and mitochondrial activity in mouse skeletal muscle cell in a
hypomagnetic field. Bioelectromagnetics 2016, 37, 212–222. [CrossRef]
43. Montoya, R.D. Magnetic fields, radicals and cellular activity. Electromagn. Biol. Med. 2017, 36, 102–113. [CrossRef]
44. Zhang, H.-T.; Zhang, Z.-J.; Mo, W.-C.; Hu, P.-D.; Ding, H.-M.; Liu, Y.; Hua, Q.; He, R.-Q. Shielding of the geomagnetic field
reduces hydrogen peroxide production in human neuroblastoma cell and inhibits the activity of CuZn superoxide dismutase.
Protein Cell 2017, 8, 527–537. [CrossRef] [PubMed]
45. Mo, W.; Liu, Y.; Bartlett, P.F.; He, R. Transcriptome profile of human neuroblastoma cells in the hypomagnetic field. Sci. China Life
Sci. 2014, 57, 448–461. [CrossRef] [PubMed]
46. Mo, W.C.; Zhang, Z.J.; Wang, D.L.; Liu, Y.; Bartlett, P.F.; He, R.Q. Shielding of the geomagnetic field alters actin assembly and
inhibits cell motility in human neuroblastoma cells. Sci. Rep. 2016, 6, 22624. [CrossRef] [PubMed]
47. Zhang, B.; Lu, H.; Xi, W.; Zhou, X.; Xu, S.; Zhang, K.; Jiang, J.; Li, Y.; Guo, A. Exposure to hypomagnetic field space for multiple
generations causes amnesia in Drosophila melanogaster. Neurosci. Lett. 2004, 371, 190–195. [CrossRef] [PubMed]
48. Sarimov, R.M.; Binhi, V.N.; Milyaev, V.A. The influence of geomagnetic field compensation on human cognitive processes.
Biophysics 2008, 53, 433–441. [CrossRef]
49. Wang, G.-M.; Fu, J.-P.; Mo, W.-C.; Zhang, H.-T.; Liu, Y.; He, R.-Q. Shielded geomagnetic field accelerates glucose consumption in
human neuroblastoma cells by promoting anaerobic glycolysis. Biochem. Biophys. Res. Commun. 2022, 601, 101–108. [CrossRef]
50. Mo, W.-C.; Zhang, Z.-J.; Liu, Y.; Bartlett, P.F.; He, R.-Q. Magnetic Shielding Accelerates the Proliferation of Human Neuroblastoma
Cell by Promoting G1-Phase Progression. PLoS ONE 2013, 8, e54775. [CrossRef]
51. Gurfinkel, Y.; At’Kov, O.; Vasin, A.; Breus, T.; Sasonko, M.; Pishchalnikov, R. Effect of zero magnetic field on cardiovascular
system and microcirculation. Life Sci. Space Res. 2016, 8, 1–7. [CrossRef]
52. IuI, G.; Vasin, A.L.; Matveeva, T.A.; Sasonko, M.L. Evaluation of the hypomagnetic environment effects on capillary blood
circulation, blood pressure and heart rate. Aviakosmicheskaia I Ekol. Meditsina= Aerosp. Environ. Med. 2014, 48, 24–30.
53. Ciorba, D.; Morariu, V.V. Life in zero magnetic field. III. Activity of aspartate aminotransferase and alanine aminotransferase
during in vitro aging of human blood. Electro- Magn. 2001, 20, 313–321. [CrossRef]
54. Katiukhin, L.N. Rheological Properties of the Erythrocytes in Weakened Static Magnetic Field of the Earth In vitro Study. J. Sci.
Res. Rep. 2019, 22, 1–12. [CrossRef]
55. Krylov, V.V.; Bolotovskaya, I.V.; Osipova, E.A. The response of European Daphnia magna Straus and Australian Daphnia carinata
King to changes in geomagnetic field. Electromagn. Biol. Med. 2013, 32, 30–39. [CrossRef] [PubMed]
56. Wan, G.-J.; Yuan, R.; Wang, W.-J.; Fu, K.-Y.; Zhao, J.-Y.; Jiang, S.-L.; Pan, W.-D.; Sword, G.A.; Chen, F.-J. Reduced geomagnetic field
may affect positive phototaxis and flight capacity of a migratory rice planthopper. Anim. Behav. 2016, 121, 107–116. [CrossRef]
57. Zhang, Y.; Pan, W. Removal or component reversal of local geomagnetic field affects foraging orientation preference in migratory
insect brown planthopper Nilaparvata lugens. Peerj 2021, 9, e12351. [CrossRef] [PubMed]Processes 2023, 11, 282 13 of 13
58. Wan, G.-J.; Jiang, S.-L.; Zhao, Z.-C.; Xu, J.-J.; Tao, X.-R.; Sword, G.A.; Gao, Y.-B.; Pan, W.-D.; Chen, F.-J. Bio-effects of near-zero
magnetic fields on the growth, development and reproduction of small brown planthopper, Laodelphax striatellus and brown
planthopper, Nilaparvata lugens. J. Insect Physiol. 2014, 68, 7–15. [CrossRef] [PubMed]
59. Mo, W.; Liu, Y.; Cooper, H.M.; He, R.-Q. Altered development of Xenopus embryos in a hypogeomagnetic field. Bioelectromagnetics
2011, 33, 238–246. [CrossRef]
60. Fesenko, E.E.; Mezhevikina, L.M.; Osipenko, M.A.; Gordon, R.Y.; Khutzian, S.S. Effect of the “zero” magnetic field on early
embryogenesis in mice. Electromagn. Biol. Med. 2010, 29, 1–8. [CrossRef]
61. Xue, X.; Ali, Y.F.; Liu, C.; Hong, Z.; Luo, W.; Nie, J.; Li, B.; Jiao, Y.; Liu, N.-A. Geomagnetic Shielding Enhances Radiation
Resistance by Promoting DNA Repair Process in Human Bronchial Epithelial Cells. Int. J. Mol. Sci. 2020, 21, 9304. [CrossRef]
62. Belyaev, I.Y.; Alipov, Y.D.; Harms-Ringdahl, M. Effects of zero magnetic field on the conformation of chromatin in human cells.
Biochim. Biophys. Acta (BBA)-Gen. Subj. 1997, 1336, 465–473. [CrossRef]
63. Baek, S.; Choi, H.; Park, H.; Cho, B.; Kim, S.; Kim, J. Effects of a hypomagnetic field on DNA methylation during the differentiation
of embryonic stem cells. Sci. Rep. 2019, 9, 1333. [CrossRef]
64. Agliassa, C.; Narayana, R.; Christie, J.M.; Maffei, M.E. Geomagnetic field impacts on cryptochrome and phytochrome signaling. J.
Photochem. Photobiol. B Biol. 2018, 185, 32–40. [CrossRef]
65. Maffei, M.E. Magnetic field effects on plant growth, development, and evolution. Front. Plant Sci. 2014, 5, 445. [CrossRef]
66. Agliassa, C.; Mannino, G.; Molino, D.; Cavalletto, S.; Contartese, V.; Bertea, C.M.; Secchi, F. A new protein hydrolysate-based
biostimulant applied by fertigation promotes relief from drought stress in Capsicum annuum L. Plant Physiol. Biochem. 2021,
166, 1076–1086. [CrossRef] [PubMed]
67. Xu, C.; Zhang, Y.; Yu, Y.; Li, Y.; Wei, S. Suppression of Arabidopsis flowering by near-null magnetic field is mediated by auxin.
Bioelectromagnetics 2017, 39, 15–24. [CrossRef] [PubMed]
68. Xu, C.; Yu, Y.; Zhang, Y.; Li, Y.; Wei, S. Gibberellins are involved in effect of near-null magnetic field on Arabidopsis flowering.
Bioelectromagnetics 2016, 38, 1–10. [CrossRef] [PubMed]
69. Mo, W.-C.; Zhang, Z.-J.; Liu, Y.; Zhai, G.-J.; Jiang, Y.-D.; He, R.-Q. Effects of a hypogeomagnetic field on gravitropism and
germination in soybean. Adv. Space Res. 2011, 47, 1616–1621. [CrossRef]
70. Xu, C.; Wei, S.; Lu, Y.; Zhang, Y.; Chen, C.; Song, T. Removal of the local geomagnetic field affects reproductive growth
inArabidopsis. Bioelectromagnetics 2013, 34, 437–442. [CrossRef]
71. Islam, M.; Maffei, M.; Vigani, G. The Geomagnetic Field Is a Contributing Factor for an Efficient Iron Uptake in Arabidopsis
thaliana. Front. Plant Sci. 2020, 11, 325. [CrossRef]
72. Negishi, Y.; Hashimoto, A.; Tsushima, M.; Dobrota, C.; Yamashita, M.; Nakamura, T. Growth of pea epicotyl in low magnetic field
implication for space research. Adv. Space Res. 1999, 23, 2029–2032. [CrossRef]
73. Xu, C.; Yin, X.; Lv, Y.; Wu, C.; Zhang, Y.; Song, T. A near-null magnetic field affects cryptochrome-related hypocotyl growth and
flowering in Arabidopsis. Adv. Space Res. 2012, 49, 834–840. [CrossRef]
74. Xu, C.; Li, Y.; Yu, Y.; Zhang, Y.; Wei, S. Suppression of Arabidopsis flowering by near-null magnetic field is affected by light.
Bioelectromagnetics 2015, 36, 476–479. [CrossRef] [PubMed]
75. Narayana, R.; Fliegmann, J.; Paponov, I.; Maffei, M.E. Reduction of geomagnetic field (GMF) to near null magnetic field (NNMF)
affects Arabidopsis thaliana root mineral nutrition. Life Sci. Space Res. 2018, 19, 43–50. [CrossRef] [PubMed]
76. Vanderstraeten, J.; Gailly, P.; Malkemper, E.P. Low-light dependence of the magnetic field effect on cryptochromes: Possible
relevance to plant ecology. Front. Plant Sci. 2018, 9, 121. [CrossRef]
77. Soltani, F.; Kashi, A.; Arghavani, M. Effect of magnetic field on Asparagus officinalis L. seed germination and seedling growth.
Seed Sci. Technol. 2006, 34, 349–353. [CrossRef]
78. Tsetlin, V.; Moisa, S.; Levinskikh, M.; Nefedova, E. EFFECT OF VERY SMALL DOSES OF IONIZING RADIATION AND
HYPOMAGNETIC FIELD CHANGE PHYSIOLOGICAL CHARACTERISTICS OF HIGHER PLANT SEEDS. Aviakosmicheskaia I
Ekol. Meditsina= Aerosp. Environ. Med. 2016, 50, 51–58. [CrossRef]
79. Zhang, S.-D.; Petersen, N.; Zhang, W.-J.; Cargou, S.; Ruan, J.; Murat, D.; Santini, C.-L.; Song, T.; Kato, T.; Notareschi, P.; et al.
Swimming behaviour and magnetotaxis function of the marine bacterium strain MO-1. Environ. Microbiol. Rep. 2013, 6, 14–20.
[CrossRef] [PubMed]
80. Poiata, A.; Creanga, D.E.; Morariu, V.V. Life in zero magnetic field. VE coli resistance to antibiotics. Electromagn. Biol. Med. 2003,
22, 171–182. [CrossRef]
81. Creanga, D.; Poiata, A.; Morariu, V.; Tupu, P. Zero-magnetic field effect in pathogen bacteria. J. Magn. Magn. Mater. 2004,
272–276, 2442–2444. [CrossRef]
82. Wang, X.K.; Ma, Q.F.; Jiang, W.; Lv, J.; Pan, W.D.; Song, T.; Wu, L.-F. Effects of Hypomagnetic Field on Magnetosome Formation of
Magnetospirillum Magneticum AMB-1. Geomicrobiol. J. 2008, 25, 296–303. [CrossRef]
83. Ilyin, V.K.; Orlov, O.I.; Morozova, Y.A.; Skedina, M.A.; Vladimirov, S.K.; Plotnikov, E.V.; Artamonov, A.A. Prognostic model for
bacterial drug resistance genes horizontal spread in space-crews. Acta Astronaut. 2022, 190, 388–394. [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual
author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to
people or property resulting from any ideas, methods, instructions or products referred to in the content.You can also read
